Assembling a safe and effective toolbox for integrated flea control and plague mitigation: Fipronil experiments with prairie dogs

Abstract

Background: Plague, a widely distributed zoonotic disease of mammalian hosts and flea vectors, poses a significant risk to ecosystems throughout much of Earth. Conservation biologists use insecticides for flea control and plague mitigation. Here, we evaluate the use of an insecticide grain bait, laced with 0.005% fipronil (FIP) by weight, with black-tailed prairie dogs (BTPDs, Cynomys ludovicianus). We consider safety measures, flea control, BTPD body condition, BTPD survival, efficacy of plague mitigation, and the speed of FIP grain application vs. infusing BTPD burrows with insecticide dusts. We also explore conservation implications for endangered black-footed ferrets (Mustela nigripes), which are specialized predators of Cynomys.

Principal findings: During 5- and 10-day laboratory trials in Colorado, USA, 2016-2017, FIP grain had no detectable acute toxic effect on 20 BTPDs that readily consumed the grain. During field experiments in South Dakota, USA, 2016-2020, FIP grain suppressed fleas on BTPDs for at least 12 months and up to 24 months in many cases; short-term flea control on a few sites was poor for unknown reasons. In an area of South Dakota where plague circulation appeared low or absent, FIP grain had no detectable effect, positive or negative, on BTPD survival. Experimental results suggest FIP grain may have improved BTPD body condition (mass:foot) and reproduction (juveniles:adults). During a 2019 plague epizootic in Colorado, BTPDs on 238 ha habitat were protected by FIP grain, whereas BTPDs were nearly eliminated on non-treated habitat. Applications of FIP grain were 2-4 times faster than dusting BTPD burrows.

Significance: Deltamethrin dust is the most commonly used insecticide for plague mitigation on Cynomys colonies. Fleas on BTPD colonies exhibit the ability to evolve resistance to deltamethrin after repeated annual treatments. Thus, more tools are needed. Accumulating data show orally-delivered FIP is safe and usually effective for flea control with BTPDs, though potential acute toxic effects cannot be ruled out. With continued study and refinement, FIP might be used in rotation with, or even replace deltamethrin, and serve an important role in Cynomys and black-footed ferret conservation. More broadly, our stepwise approach to research on FIP may function as a template or guide for evaluations of insecticides in the context of wildlife conservation.

Fig 1. Predicted body condition indices (mass:foot) for black-tailed prairie dogs at South Exclosure and Big Foot Road colonies, South Dakota, USA, 2017.

At each colony, data were collected on paired sites treated with 0.005% fipronil (FIP) grain on 24 Jul or left non-treated. Data were collected during 3 BACI (before-after-control-impact) periods: Before FIP grain treatments (June-24 July), After-1 (25 July-30 August), and After-2 (1 September-October). Here, prairie dog ages/sexes are combined for simplicity. Error bars are ± 1 SE.

Fig 2. Predicted body condition indices (mass:foot) for black-tailed prairie dogs at Prairie Wind and South Exclosure colonies, South Dakota, USA, 2018.

Two sites at the South Exclosure were treated with 0.005% fipronil (FIP) grain on 23 July. Data were collected during 3 BACI (before-after-control-impact) periods: Before FIP grain treatments (June-22 July), After-1 (25 July-30 August), and After-2 (1 September-October). Here, prairie dog ages/sexes are combined for simplicity. Error bars are ± 1 SE.

Fig 3. Predicted densities of black-tailed prairie dogs (BTPDs) ha^-1 in 2018 (before plague epizootic) and 2020 (after epizootic) on habitats with differing plague treatments including non-treated (baseline) and 0.005% fipronil (FIP) grain, Rocky Mountain Arsenal National Wildlife Refuge, Colorado, USA.

Error bars are ± 1 SE.

Fig 4. Cumulative precipitation (mm) at Rocky Mountain Arsenal National Wildlife Refuge, Colorado, USA, 2018–2020.

The historic average, from 1895–2020 (https://www.prism.oregonstate.edu/), is depicted as a dashed line for reference. Also worthy of note, winter weather was considered extreme in November and December 2019, when an Arctic airmass brought frigid temperatures and snowfall.